Feeding Ecology and Conservation Biology of the Black

Snub-nosed Monkey (Rhinopithecus strykeri)

Yin YANG

A thesis submitted for the degree of

Doctor of Philosophy of the Australian National University

June 2019

© Copyright by Yin Yang 2019

a

Painting by Xu Ling b

Statement of Originality

The work presented in this thesis is, to the best of my knowledge and belief, original and my own work except where otherwise acknowledged or where reference is made in the text. This dissertation has not been submitted either in whole or in part, for a degree at this or any other university. This dissertation is structured as a series of connected papers that have been published (Chapter 5, 6, 7, 8 and 9) or is in preparation (Chapter 3) for publication at the time of thesis submission. As each chapter is an individual manuscript, some repetition occurs, particularly in the introductions, and there are inconsistencies in style and formatting.

Yin YANG

10th June 2019

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Acknowledgments

I am very grateful for the financial support provided by the Australian National University

(ANU) [ANU Fieldwork Funding for Higher Degree Research (HDR) Students, R61250FW;

ANU Vice-Chancellor's HDR Travel Grant, 4885859], Zoological Society for the

Conservation of and Populations (ZGAP) (Germany, Rhinopithecus.MMR.2015) and the Institute of Eastern-Himalaya Biodiversity Research (IEHBR). Without the grants from these institutes, this Ph.D. project would be neither launched nor completed. I thank the

Yunnan Provincial Forestry and Grassland Administration, Nujiang Administration Bureau and Lushui Bureau of Gaoligong Mountains National Nature Reserve for giving me permission and all necessary assistance in conducting a population survey of, and conservation projects for, the black snub-nosed monkey at Gaoligong Mountains in Nujiang

Autonomous Prefecture, .

This research was conducted in accordance with the guidelines of the

Experimentation Ethics Committee of the Australian National University (A2015/04).

Without numerous people providing passionate help and strong scientific or logistical support, this dissertation would not have been successful.

A special and hearty thanks firstly goes to members of my supervisor panel:

Dr. Alison Behie gave guidance and support on my work all the way from the initial to the final step. Her patience and invaluable feedback helped me greatly in completing this PhD project. She also assisted in framing the structure of this dissertation, helped me concentrate on the topics handled in this dissertation, and examined my final dissertation for submission.

I also thank her for believing in me and allowing me to freely pursue and carry on research into my own interests. ii

Prof. Colin Groves guided me at every turn, from the field of forestry to primatology - and he introduced me to Dr. Alison Behie. He always gave me enough encouragement to overcome difficulties in this project and kept on believing in the success of my project. He introduced me to staffs in ZGAP and thus I received the first research funding of my career. His continuous and always-immediate feedback improved this work and my knowledge on considerably. Even just two weeks before he passed away, I received his detailed comments and a revised version of our manuscript with further encouragement of my work.

Being able to be one of his students is one of the greatest honours in my life. I sorely miss him, my mentor and scientific supervisor. This work is dedicated to Prof. Colin Goves.

Prof. Xiao Wen invited me to be a visiting student to his lab in IEHBR. He also introduced me to the field sites, field guides, and staffs of the Administration Bureau of Gaoligong

Mountains National Nature Reserve. He gave me regular advice on all aspects of my project and shared with me his data for conducting the habitat evaluation process of the black snub- nosed monkey and other endangered species in Gaoligong Mountains Region. Also, partial grants from him made this project possible.

Prof. Long Yongcheng first inspired me with his efforts on black-and-white snub-nosed monkey conservation over the past 20 years and introduced me to Prof. Xiao Wen and other scholars in the China Primatological Society. He also gave me enthusiastic encouragement on my work and constantly provided ideological support towards my scientific publications.

Prof. Paul A. Garber, my external advisor, also provided endless motivation and a very strong intellectual contribution (extensive discussion, comments, revision and proof reading) on numerous publications and chapters, particularly Chapters 3, 5, 6, 7, and 9.

I also express my thanks to:

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Dr. Ren Guopeng for offering me unparalleled assistance and advice regarding my use of statistics and data analysis, especially his contributions on habitat modelling.

Dr. Huang Zhipan and Dr. Ma Chi for collecting interview-based data and providing them for the modelling in Chapters 8 and 9.

Dr. Li Qihua for opening his lab to me and his invaluble contributions in laboratory work on nutrition analysis.

Dr. Cyril C. Grüter for extensively commenting on and improving the quality of Chapters 3 and 7.

Dr. Rebecca L. Hendershott for her proof reading and English editing.

Prof. Jessica M. Rothman, Dr. Craig Kirkpatrick, Dr. Yi Shaoliang, Tilo Nalder, Guy M.

Williams and several anonymous reviewers for instructive comments on the content of various manuscripts and texts.

Frank Momberg, Ngwe Lwin, and Aung Ko Lin for sharing their data of the black snub- nosed monkey and other related biodiversity data from .

Roland Wirth at ZGAP for helps to bridge relationship and coordinate supports and funding to me.

Dr. Liang Dan and Chen Yixin for exchanging information on our common interests of

Gaoligong Mountains' biodiversity and conservation.

Gao Yin for assisting me to illustrate the GIS maps and run models when I was unable to access my data stored on the office computer.

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Wang Xinwen, Li Guangsong, Wang Bin, Tian Yingping for their logistics and hospitable assistance for my field research.

My colleagues, Dong Shaohua, Keng-Hua Niu-ba, A Feng-Hua, for their field assistance and hard work in searching for the Luoma population in the Gaoligong Mountains. I will never forget that they insisted on searching for me and found me in the mountains at around 3 am at an elevation of approximate 3100 m in winter when I got lost in the on 8th January

2016. They really saved my life!

Peng Peixing and Ou Xuejun, keepers in Yaojiaping Wildlife Rescue Centre, for their great effort in rearing the captive black snub-nosed monkeys and cooking for me when I came back from the mountains.

I wish to express my respect to the eminent botanist Professor Li Hen (KNU), who conducted research and collected > 30,000 plant specimens over the past 30 years in the Gaoligong

Mountains and generously allowed me to use her collections for this project. Without her help and hard work in this remote region, I could not have completed this research.

The classification of plant species was completed with the assistance of Dr. Qing Jiali and Dr.

Li Shuangzhi (Southwest Forestry University), Dr. Fang Ruizheng (KUN, spp. and Vacciniaceae species), Dr. Li Xiwen (KUN, species), Dr. Li Rong (KUN,

Schefflera spp. and Orchidaceae species), Dr. Wang Lisong and Ms. Shi Haixia (lichen species). Dr. Fang Wei provided facilities for identification of our specimens in KUN.

Lastly, I am immensely grateful for my (Mo Songlin, Ding Fngfang and Yang Jinqiu) for their love and patience in me and wholehearted support of my intellectual pursuits.

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Table of Contents

Statement of Originality ...... i

Acknowledgments...... ii

Table of Contents ...... vi

Abstract ...... xiii

List of Figures ...... xvi

List of Tables ...... xviii

Abbreviations ...... xix

Chapter 1 Introduction ...... 1

1 General Introduction ...... 1

1.1 Background to the Current Research ...... 1

1.2 Research Limitations ...... 3

1.3 Outline of Dissertation ...... 3

Reference ...... 5

Chapter 2 Literature Review ...... 7

2 Introduction to Colobines ...... 7

2.1 and Distribution of Colobines in China ...... 7

2.2 Evolutionary History of Asian Colobines ...... 9

2.3 Behavioural Ecology ...... 11

2.3.1 Feeding ecology of colobines ...... 11 2.3.2 Ranging behaviours of colobines ...... 19 2.3.3 Social organisation of colobines ...... 26 2.4 Chinese Colobines ...... 27

2.5 General Introduction to Snub-Nosed Monkeys ...... 28

2.5.1 Distribution and conservation status of snub-nosed monkeys ...... 29 2.5.2 Taxonomy and evolution of snub-nosed monkeys ...... 31 2.5.3 Social organisation of snub-nosed monkeys ...... 32 vi

Reference ...... 36

Chapter 3 Lichenivory and Ecological-Constraints in (Temperate) Snub-Nosed Monkeys ... 60

3 Introduction ...... 60

3.1 A Review of the Feeding Ecology of Snub-Nosed Monkeys ...... 61

3.1.1 Dietary diversity, dietary selectivity and seasonal dietary patterns ...... 61 3.1.2 Nutritional chemistry...... 73 3.2 A Review of Ranging Behaviours of Snub-Nosed Monkeys ...... 75

3.3 Methods...... 81

3.3.1 Literature review ...... 81 3.3.2 Statistical analyses...... 82 3.4 Results ...... 83

3.4.1 Snub-nosed monkeys living at higher elevations have higher rates of licheivory ...... 83 3.4.2 Ecological constraints model unsupported in temperate snub-nosed monkeys ...... 85 3.4.3 Seasonal changes in snub-nosed monkey ranging patterns ...... 86 3.5 Discussion ...... 91

3.5.1 Summary of results...... 91 3.5.2 Function of lichen feeding ...... 92 3.5.3 Significance of daily range length and home range dimension ...... 93 3.5.4 Lichenivory as a preferred dietary resource for temperate snub-nosed monkeys ...... 94 Reference ...... 98

Chapter 4: The Natural History and Conservation Status of the Black Snub-Nosed Monkeys ...... 111

4 An Introduction to the Black Snub-Nosed Monkeys ...... 111

4.1 Morphological Characteristics and Life History ...... 111

4.2 Geographic Distribution and Population Status ...... 114

4.3 Habitat and Environment ...... 116

4.3.1 The Gaoligong Mountains ...... 116

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4.3.2 Climate ...... 117 4.3.3 Habitat vegetation ...... 118 4.4 Social Organisation and Ranging Patterns ...... 124

4.5 Conservation Assessment ...... 125

4.5.1 Poaching pressure ...... 126 4.5.2 Logging and deforestation ...... 128 Reference ...... 131

Chapter 5 The Critically Endangered Black Snub-Nosed Monkey Rhinopithecus strykeri Found in the Salween River Basin, China ...... 135

References ...... 139

Chapter 6 First Insights into the Feeding Habits of the Critically Endangered Black Snub- Nosed Monkey Rhinopithecus strykeri (, ) ...... 141

6.1 Introduction ...... 141

6.2 Methods...... 144

6.2.1 Study site ...... 144 6.2.2 Feeding study of the wild black snub-nosed monkeys ...... 145 6.2.3 Cafeteria-style feeding trials ...... 147 6.2.4 Measuring wild plant species distribution patterns ...... 149 6.3 Results ...... 151

6.3.1 Diet o